Role of the Medial and Lateral Caudate-Putamen in Mediating an Auditory Conditional Response Association

doi:10.1006/nlme.2000.3989

Neurobiology of Learning and Memory

Volume 76, Issue 1, July 2001, Pages 106-116

https://doi.org/10.1006/nlme.2000.3989 Get rights and content

Abstract

Rats with quinolinic acid lesions of the medial or lateral caudate-putamen (CPu) and controls were tested for performance of a previously learned auditory conditional response association task. The task involved the selection of two possible responses when presented with one of two different tones. Results indicated that lesions of either the medial or the lateral CPu produced a sustained deficit in the auditory conditional response association task. Only the lateral CPu lesioned rats exhibited transient motor problems immediately following surgery, but these problems did not interfere with the execution of the appropriate responses. It is suggested that both the medial and the lateral CPu are involved in response selection and response separation within egocentric space.

References (29)

D. Cook et al.
Caudate nucleus and memory for egocentric localization
Behavioral & Neural Biology
(1988)
B.D. Devan et al.
Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: Relation to thigmotaxis
Behavioural Brain Research
(1999)
R.A. Fricker et al.
The placement of a striatal ibotenic acid lesion affects skilled forelimb use and the direction of drug-induced rotation
Brain Research Bulletin
(1996)
J.C.S. Furtado et al.
Behavioral characterization of quinolinate-induced lesions of the medial striatum: Relevance for Huntington's disease
Experimental Neurology
(1996)
C.R. Gerfen et al.
The basal ganglia
A.M. Graybiel
The basal ganglia and chunking of action repertories
Neurobiology of Learning and Memory
(1998)
W. Hauber et al.
Differential effects of lesions of the dorsomedial and dorsolateral caudate-putamen on reaction time performance in rats
Behavioural Brain Research
(1994)
M.G. Packard et al.
Lesions of the caudate nucleus selectively impair “Reference Memory” acquisition in the radial maze
Behavioral & Neural Biology
(1990)
M. Pisa
Motor functions of the striatum in the rat: Critical role of the lateral region in tongue and forelimb reaching
Neuroscience
(1988)
M. Pisa et al.
Regionally selective roles of the rat's striatum in modality-specific discrimination learning and forelimb reaching
Behavioral Brain Research
(1990)

P.J. Reading et al.

Dissociable roles of the ventral, medial and lateral striatum on the acquisition and performance of a complex visual stimulus-response habit

Behavioural Brain Research

(1991)

I.Q. Whishaw et al.

Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats

Behavioral Brain Research

(1987)

P.J. Brasted et al.

Unilateral lesions of the dorsal striatum in rats disrupt responding in egocentric space

Journal of Neuroscience

(1997)

P.J. Colombo et al.

Allocentric spatial and tactile memory impairments in rats with dorsal caudate lesions are affected by preoperative behavioral training

Behavioral Neuroscience

(1989)

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Cortical motor areas are influenced not only by peripheral sensory afferents and prefrontal association areas, but also by the basal ganglia, specifically the striatum. The dorsomedial striatum (DMS) and dorsolateral striatum are involved in both spatial and stimulus-response learning; however, each of these areas may mediate different components of learning. The aim of the study is to determine the effect of electrolytic lesion to the DMS on the learning and performance of sexual behaviour and locomotor activity in male rats.
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Procedural learning and memory involves the acquisition, consolidation, and retrieval of individual representations that are behaviorally expressed in an inflexible manner. Stimulus–response habit learning represents a prominent form of procedural learning in the mammalian brain. Extensive evidence supports the hypothesis that this form of procedural learning is mediated by a neural system that contains the dorsal striatum as a primary component. Studies employing brain lesion techniques have dissociated the roles of the dorsal striatum and hippocampus in procedural and declarative memory, respectively. Pharmacological studies indicate a selective role for dorsal striatal dopamine, acetylcholine, glutamate, and cannabinoids in stimulus–response procedural learning.
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Citation Excerpt :
Indeed, several experiments using food reward suggest a role of the DLS in the performance of learned S–R associations, but not in relational “place” learning. For example, post-acquisition lesions of the DLS affect simple discrimination learning (Adams, Kesner, & Ragozzino, 2001; Broadbent, Squire, & Clark, 2007; Featherstone and McDonald, 2005) and egocentric spatial learning (Cook & Kesner, 1988), but do not affect performance in a conditioned place preference task (Featherstone and McDonald, 2005) or allocentric spatial learning (Cook & Kesner, 1988). Furthermore, using a two-choice discrimination task, Broadbent et al., 2007 showed the olfactory version was acquired more quickly than either objects or patterns and was also most affected by post-acquisition DLS lesions.
Animals can use multiple strategies when learning about, and navigating within, their environment. Typically, in the frequently-studied food-rewarded T-maze, rats initially adopt a flexible, hippocampal-dependent place strategy. However, as learning progresses, rats switch to an automatic, striatal-dependent response strategy (Packard & McGaugh, 1996). Interestingly, in a similar but aversively motivating water-submerged T-maze, rats exhibit the opposite behavioral pattern, initially adopting a response strategy but switching to a place strategy with extended training (Asem & Holland, 2013). Here, we examined the effects of transient lidocaine inactivation of the dorsolateral striatum (DLS) on rats’ acquisition and expression of place and response strategies in the submerged T-maze. DLS inactivation prior to probe tests had no effect on rats’ initial expression of a response strategy nor on their transition to the use of a place strategy with further training. Nevertheless, in a second experiment using the same rats, identical inactivation parameters significantly affected performance in an appetitively motivating positive control task, which required a response strategy. Furthermore, in a third experiment, DLS inactivation prior to early learning trials interfered with the acquisition of the response strategy in the submerged T-maze. These differences in DLS inactivation effects across appetitive and aversive tasks support the view that task motivation plays crucial roles in guiding learning, memory, and behavior. Additionally, differences in DLS inactivation effects between tests of acquisition and expression suggest that the DLS is required during early acquisition but not expression of the response learning strategy.
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In these cases, damage to the striatum, but not the hippocampus, should selectively disrupt task learning and performance. In support of this view, damage to the dorsal striatum impairs both the acquisition (Featherstone & McDonald, 2005; Winocur & Eskes, 1998) and post-learning retention (Adams, Kesner, & Ragozzino, 2001) of elemental CD tasks that can be solved using a stimulus-response strategy. Conditional discrimination tasks that require a spatial response, such as tasks in which a conditional cue is associated with the location of a reward on a maze, are a particular variant of CD problem that is less well characterized with regard to the involvement of the dorsal hippocampus (DH) and dorsal striatum (DS).
The roles of the dorsal hippocampus (DH) and dorsal striatum (DS) in the learning and retention of conditional discrimination (CD) rules is a subject of debate. Although previous studies have examined the relationship between the DH and DS and the performance of CD tasks in operant chambers, the relative contributions of these two brain regions to the retention of CD rules requiring an association between a cue and a spatial location have not been characterized. We designed an experiment to assess the roles of the DH and DS in the retention of a visuospatial CD task by transiently inactivating either structure with muscimol in separate groups of rats and measuring performance on a previously learned CD task. The performance of two other groups of rats on a previously learned delayed spatial alternation (DA) task was also measured following inactivation of either DS or DH, which allowed us to control for any possibly confounding effects of spatial cues present in the testing room, length of the intertrial interval period on the performance of the CD task, and muscimol on sensorimotor or motivational processing. Muscimol inactivation of dorsal striatum, but not dorsal hippocampus, impaired CD performance, while inactivation of dorsal hippocampus, but not dorsal striatum impaired DA performance. These results demonstrate a double dissociation between the roles of the DH and DS in these two tasks, and provide a systematic characterization of the relationship between these two brain areas and CD performance.

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^☆: This research was supported by NIH Grant 2RO1NS20771-13 and NSF Grant BNS 892-1532.

^f2: Address correspondence and reprint requests to Raymond P. Kesner, University of Utah, Department of Psychology, 380 South 1530 East, Room 502, Salt Lake City, UT 84112-0251. Fax: (801) 581-5841. E-mail: [email protected].

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Regular ArticleRole of the Medial and Lateral Caudate-Putamen in Mediating an Auditory Conditional Response Association☆

Abstract

Behavioral & Neural Biology

Behavioural Brain Research

Brain Research Bulletin

Experimental Neurology

Neurobiology of Learning and Memory

Behavioural Brain Research

Behavioral & Neural Biology

Neuroscience

Behavioral Brain Research

Behavioural Brain Research

Behavioral Brain Research

Unilateral lesions of the dorsal striatum in rats disrupt responding in egocentric space

Journal of Neuroscience

Allocentric spatial and tactile memory impairments in rats with dorsal caudate lesions are affected by preoperative behavioral training

Behavioral Neuroscience

Regular Article
Role of the Medial and Lateral Caudate-Putamen in Mediating an Auditory Conditional Response Association☆